Assessing postzygotic isolation using zygotic disequilibria in natural hybrid zones.

Xin-Sheng Hu,Francis C Yeh

doi:10.1371/journal.pone.0100568

Abstract

Hybrid zones as windows on evolutionary processes provide a natural laboratory for studying the genetic basis and mechanisms of postzygotic isolation. One resultant pattern in hybrid zones is the Hardy-Weinberg disequilibrium (HWD) for a single locus or the linkage disequilibrium (LD) for multiple loci produced by natural selection against hybrids. However, HWD and the commonly used low-order gametic or composite digenic LD cannot fully reflect the pattern of the high-order genotypic interactions. Here we propose the use of zygotic LD to elucidate the selection mechanisms of postzygotic isolation, and its calculation is based on genotypic frequencies only, irrespective of the type of mating system. We numerically and analytically show that the maximum composite digenic LD is always greater than the maximum absolute zygotic LD under the linear-additive selection, but is comparable to or smaller than the maximum absolute zygotic LD under the strong epistatic selection. Selection mechanisms can be inferred by testing such differences. We analyze a previously reported mouse hybrid zone assayed with genome-wide SNPs, and confirm that the composite digenic LD cannot appropriately indicate all possible significant genotypic interactions for a given SNP pair. A large proportion of significant zygotic LDs, ∼75% in general in the mouse hybrid zone, cannot be revealed from the composite digenic LD analysis. Statistical tests indicate that epistatic selection occurred among multiple loci in the mouse hybrid zone. The results highlight that the joint patterns of the composite digenic and zygotic LDs can help to elucidate the selection mechanism that is potentially involved in postzygotic isolation.

Highlights

Postzygotic isolation occurs when the hybrids produced by two genetically diverging species in sympatry are successfully formed but eventually turn out to be inviability or sterility [1]
We propose the use of zygotic linkage disequilibrium (LD) to characterize genotypic interactions and compare its pattern with that of the composite digenic LD in a hybrid zone where two genetically diverging species are partially integrated through hybridizations
It is clear that the composite digenic LD measures the non-random associations of two alleles, and can be affected by selection at either the gametophyte stage or sporophyte stage, or both

Summary

Introduction

Postzygotic isolation occurs when the hybrids produced by two genetically diverging species in sympatry are successfully formed but eventually turn out to be inviability or sterility [1]. In flowering plants, this takes place in the sporophyte stage where ovules of one species and pollen from the other species are fused to produce zygotes, irrespective of the presence or absence of prezygotic isolation. An observable pattern for a single locus is the likely significant Hardy-Weinberg disequilibrium (HWD) due to heterozygous deficiency in the hybridizing populations. The current availability of genome-wide single nucleotide polymorphisms (SNPs) provides us with an opportunity to use genome-wide pattern of LD to study the genetic basis and mechanisms of speciation [9], [10], [11], [12], [13]

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Conclusion